Insect. Soc. DOI 10.1007/s00040-016-0503-1 Insectes Sociaux

RESEARCH ARTICLE

Queen location and nest site preference influence colony reunification by the rugatulus

1 2 G. N. Doering • S. C. Pratt

Received: 10 May 2016 / Revised: 2 August 2016 / Accepted: 3 August 2016 Ó International Union for the Study of Social (IUSSI) 2016

Abstract Social colonies adeptly make consensus Introduction decisions that emerge from distributed interactions among colony members. How consensus is accomplished when a Group-living frequently confront decisions that split decision requires resolution is poorly understood. We require consensus on a single option (Camazine et al. 2001; studied colony reunification during emigrations of the cre- Conradt and Roper 2005; Dyer et al. 2008; Kameda et al. vice-dwelling ant . Colonies can 2012). This need is particularly clear for movement deci- choose the most preferred of several alternative nest cavi- sions, such as the choice of a new nest site by an emigrating ties, but the colony sometimes initially splits between sites ant or bee colony (Visscher 2007; Seeley 2010; Pratt 2010). and achieves consensus later via secondary emigrations. We While a colony may benefit from dividing among sites explored the decision rules that govern reunification using (Debout et al. 2007; Robinson 2014), the costs of separating artificially split colonies. When monogynous colonies were the queen from part of her workforce include depriving her evenly divided between identical sites, the location of the of their labor and might lower both queen and worker queen played a decisive role, with 14 of the 16 colonies inclusive fitness. reuniting at the site that held the queen. This suggests a Emigrating colonies possess effective means of achiev- group-level strategy for minimizing risk to the queen by ing consensus, despite lacking well-informed leaders that avoiding unnecessary moves. When the queen was placed in can impose a single best choice on the entire group (Seeley the less preferred of two sites, all 14 colonies that reunited 2010; Pratt 2010; Kaur et al. 2012; Cronin 2012). A decision did so at the preferred nest, despite having to move the instead emerges from competition among locally informed queen. These results show that colonies balance multiple individuals, each of which promotes one option. The factors when reaching consensus, and that preferences for effectiveness of this promotion correlates with that option’s physical features of the environment can outweigh the quality (Seeley and Buhrman 2001; Mallon et al. 2001; queen’s influence. Robinson et al. 2011). Quality-dependence does not by itself lead to consensus, but social insects have evolved additional Keywords Consensus decision making Á mechanisms that do so, including quorum rules and highly Nest site selection Á Emigration Á Queen Á Temnothorax nonlinear responses to recruitment signals (Pratt et al. 2002; Seeley and Visscher 2003; Pratt 2005; Sumpter and Pratt 2009; Cronin 2012). These tactics amplify differences in the popularity of competing options, so that recruitment to one site eventually dominates the others. Leaderless colonies & G. N. Doering can thereby cohesively move to a single site and also reach [email protected] consensus in other contexts, such as foraging, escape from 1 School for Engineering of Matter, Transport and Energy, danger, and nest building by self-assembly (Nicolis and Arizona State University, Tempe, AZ, USA Deneubourg 1999; Camazine et al. 2001; Lioni and 2 School of Life Sciences, Arizona State University, Tempe, Deneubourg 2004; Altshuler et al. 2005; Pratt et al. 2005; AZ, USA Detrain and Deneubourg 2008; Seeley 2010; Cronin 2013). 123 G. N. Doering, S. C. Pratt

Consensus-building mechanisms are well illustrated by albipennis take special precautions to protect the queen; in the emigration behavior of Temnothorax . These insects migrations she is moved toward the middle of the emigra- typically live in preformed cavities such as hollow nuts or tion. This ensures that she always has the protection of rock crevices, and colonies are adept at emigrating to the roughly half of the colony’s workers (Franks and Sendova- best of several alternatives when their old nest is damaged Franks 2000). It is, therefore, reasonable to expect that or when a better site becomes available (Franks et al. 2002; colonies might act similarly to minimize danger to the Dornhaus et al. 2004; Pratt 2010). Decision-making relies queen during reunification. on quality-dependent initiation of tandem run recruitment, To investigate reunification, we split colonies of T. in which a scout leads a single nestmate to a promising rugatulus between two sites and allowed them to reunite, candidate home (Mallon et al. 2001; Robinson et al. 2011). noting which site they chose. To test for an effect of queen Recruitment generates positive feedback through site pop- location we divided monogynous colonies between two ulation, and does so more effectively for better sites. The identical nests and randomly assigned the queen to one of quality effect is amplified by a quorum rule under which them. We then compared the relative influence of queen slow tandem recruitment is succeeded by speedier social location and site design by placing these criteria in conflict; transport when a site population exceeds a threshold (Pratt we divided colonies between two nests that differed in et al. 2002). The winning site is likely to be the best one, cavity brightness and placed the queen in the brighter, less because quality-dependent recruitment means that better preferred site. We subsequently observed the ants’ choices sites attain a quorum earlier (Pratt et al. 2005; Pratt and to determine whether they weighed one criterion over the Sumpter 2006; Sumpter and Pratt 2009). Once the ants other. Queen number varies widely in T. rugatulus (Ru¨ppell accelerate migration by switching to transport, they are et al. 2001; Heinze and Ru¨ppell 2014), but we focused on likely to complete the move before any competing sites monogynous colonies, because we expected that protection reach a quorum. of their only queen might be especially important. While the ants’ decision algorithm minimizes split decisions, it does not completely avoid them. Emigrating colonies sometimes transiently occupy multiple sites before Methods reuniting at a single home (Franks et al. 2003a; Pratt and Sumpter 2006; Franks et al. 2008). These splits reflect a Nest designs tension between colony cohesion and rapid movement, and they become more likely when dangerous conditions require Nests consisted of a 2.4 mm thick balsa wood slat placed a colony to move quickly (Pratt and Sumpter 2006; Franks between two glass microscope slides (50 9 75 mm). A et al. 2013). At a mechanistic level, splits occur when more circular hole drilled through the center of the slat created a than one site simultaneously attains a quorum, triggering 38 mm diameter nest cavity, accessible to the ants by a social transport to multiple sites. Reunification requires a 2 mm wide slit through one side of the slat. To dim the second stage of emigration in which all but one of the cavity interior and make the nests more attractive to the occupied sites are abandoned in favor of a single winner. ants, neutral density filters (Rosco Cinegel) were sand- The criteria that govern which site wins and the behavior wiched between two microscope slides and placed on top of that allows reunification of the colony remain poorly the nest. We used a single 1-stop filter in all nests except for understood. the dimmer nests in the second experiment, which were In this study we investigated the influence of two fitted with three 3-stop filters. Balsa slats were discarded potential reunification criteria: The physical features of the after each experiment, but slides were re-used after cleaning occupied sites and the location of the queen. We expected in a commercial dishwasher. See Sasaki et al. (2015) for that colonies should attend to site features, just as they do in further details on nest construction. the initial phase of emigration. Preference tests have shown that Temnothorax base their decisions on several factors, Subjects including entrance size, interior light level, and the height and area of the nest cavity (Pratt and Pierce 2001; Mallon The same 18 colonies were used in both the first and second et al. 2001; Franks et al. 2003b; Visscher 2007; Mitrus experiments; an additional two colonies were used only in 2014). We further hypothesized that colonies prefer the site the second experiment. All colonies had a single queen, that holds the queen, to avoid moving her from one site to 50–150 workers, and 0–50 brood items. This size range is the other. Exposure during emigration is dangerous (Ret- similar to that seen in other studies of nest-site selection by tenmeyer et al. 1978; Franks and Sendova-Franks 2000; Temnothorax (e.g. Dornhaus et al. 2004; Robinson et al. Dornhaus et al. 2004; Bouchet et al. 2013) and the queen’s 2009; Sasaki et al. 2015). Colonies were collected in the survival is vital to the colony’s future fitness. Temnothorax Pinal Mountains of Arizona (33.317N 110.876W) in May 123 Queen location and nest site preference influence colony reunification by the ant… and September of 2013 and 2014. Before the start of the experiments, colonies lived in nests like those described Arena above but without the neutral density filters. Each nest was housed in its own 11 9 11 cm plastic box. Colonies were fed weekly with an agar-based diet (Bhatkar and Whitcomb 1970), and nest boxes were also provided with water tubes that were refilled weekly. Voucher specimens from each colony were deposited at the Arizona State University Natural History Collections in Tempe, Arizona.

Experiment 1: effect of queen Nests In this experiment we evenly divided each colony between two identical nests. We first placed the two nests into sep- 5 cm arate circular plastic arenas (24 cm diameter, 9 cm height), Fig. 1 Setup for reunification experiments. Colonies were evenly whose walls were coated with Fluon to prevent ants from divided between two artificial nests placed approximately 6 cm apart escaping. The colony, still in its home nest, was placed into in a circular arena a third arena of the same design. We removed the roof of the home nest and waited 1–3 min, during which period some other on the same bench. In one member of each pair the workers left the nest and wandered the arena. We took these queen was initially in the left nest, while in the other she was ants to be the active scouts that find, assess, and recruit to in the right nest. This controlled for any directional biases candidate sites, while the passive majority of the colony created by asymmetries of lighting or visual cues. Asym- waits at the old nest to be transported. We used soft forceps metries were also minimized by performing the experiment to evenly distribute the active ants, one-by-one, between the in an environmental growth chamber evenly illuminated by two target nests. We then similarly divided the ants that had overhead fluorescent lamps. If a colony was still split remained within the nest, as well as the brood items. Pupae between the two sites at the end of observations, it was and larvae were moved one at a time using soft forceps. induced to reunify by removing the roofs of both sites and Eggs were too delicate to be grasped like this, but they providing an intact third site nearby. In some cases, colonies would adhere to the tip of moistened forceps (or the head of that did not re-unite were re-tested at a later date, up to a an insect pin) gently pressed against them. In this way, maximum of three times. We waited at least one full day clumps of eggs could be moved together. This approach before re-testing a colony. This experiment was conducted ensured that each nest had a roughly similar balance of in April 2015. active scouts, passive ants, and brood. Finally, the queen was randomly assigned to one of the two nests, using Experiment 2: effect of nest site design Wolfram Alpha’s virtual coin flip function (http://www. wolframalpha.com). In this experiment colonies were evenly split between two Colonies were given a few hours to move into their new nests that differed in a physical feature known to influence nests, which were then placed in a single test arena with their the ants’ site preferences. The nests were identical except entrances facing one another at a distance of approximately for interior light level, achieved using three 3-stop filters in 6cm(Fig.1). The test arena, like those used to split the the roof of the better site versus a single 1-stop filter for the colonies, was first cleaned with ethanol to minimize cues that worse site [Temnothorax ants consistently prefer darker might bias the ants’ decisions. Ants that were outside of the nests in choice tests (Franks et al. 2003b, 2006; Pratt and nests were also transferred to the test arena. Twenty hours Sumpter 2006)]. The queen was always assigned to the later, we noted the nest at which the colony had reunited. A brighter nest. Methods followed those of Experiment 1, colony was described as reunified if at least four fifths of its except for the following differences: (1) instead of using members were found in one of the two nests. Reunification forceps to divide each colony one ant at a time, we took an was also video-recorded with a Panasonic camcorder (HC- approximate count of the number of workers in each nest V520M) mounted on a copy stand approximately 60 cm and then used a soft tipped paintbrush to split the ants above the arena. Colonies were split in the morning, and roughly evenly between the two nests; (2) no colony was placed in the test arena in the mid to late afternoon. tested more than once, even those that failed to re-unite. On each day of the experiment, two colonies were tested This experiment was conducted in February and March of simultaneously in identical setups placed adjacent to each 2015.

123 G. N. Doering, S. C. Pratt

Results 16 14 Experiment 1: effect of queen 12 Of the 18 colonies tested, nine reunited on their first trial, 10 five on their second trial, and two on their third trial. The 8 remaining two did not reunite, instead remaining roughly 6 evenly split between the sites. Of the 16 colonies that reunited, 14 did so at the nest containing the queen, a sig- 4 Number of Colonies nificant preference (2-tailed binomial test: p = 0.004). If we 2 consider the two non-reuniting colonies as being indifferent 0 between the sites, we can assign one to each choice, giving a Reunited Reunited Did not total of 15 for the queenright nest and three for the queenless at dimmer at brighter reunite nest. This still indicates a significant preference for the nest nest queenright nest (p = 0.008) (see Fig. 2).

Experiment 2: effect of nest site design Fig. 3 Results of Experiment 2. Bar heights give the total number of colonies reuniting at the dimmer nest, reuniting at the brighter nest, or failing to reunite Of the 20 colonies tested, six did not reunite, instead remaining roughly evenly split between the sites, as in experiment 1. All adaptation for minimizing danger to the queen, whose egg- of the 14 colonies that did reunite chose the darker, queenless laying role makes a unique contribution to the entire col- nest over the brighter, queenright nest, a significant preference ony’s inclusive fitness. Colonies may benefit from a (2-tailed binomial test: p = 0.0001). As before, if we consider reunification strategy that minimizes the queen’s exposure the six non-reuniting colonies to be indifferent, we can evenly to potentially harmful environmental extremes and risks of divide them between the two choices, giving a total of 17 predation. This behavior differs from that of the ponerine choices for the darker nest and three for the brighter nest. This ant Diacamma indicum, for which the location of repro- pattern still indicates a significant preference for the darker ductive individuals did not determine where divided nest (p = 0.003) (see Fig. 3). colonies reunite (Kaur et al. 2012). The reproductives of D. indicum, however, are not queens but gamergates, mated Discussion workers that can readily be replaced. A T. rugatulus colony that has lost its queen might also be able to rear a new one, Monogynous colonies of Temnothorax rugatulus, when as this shows evidence of re-adoption of newly ¨ evenly divided between identical nests, reunited at the nest mated queens into their natal nests (Ruppell et al. 2001). that contained their queen. This may be a group-level Rearing a new queen takes weeks or months, hence these ants may be under stronger selection to protect the queen 16 they already have. Similar selective pressures have been argued to account for the timing of queen movement by T. 14 albipennis colonies, which typically bring her from the old 12 nest to the new about halfway through the emigration 10 (Franks and Sendova-Franks 2000). Movement earlier or 8 later might increase the queen’s risk of harm by leaving her behind in a nearly abandoned nest or moving her prema- 6 turely to a barely populated one. Like the decision rule 4 reported here, this timing strategy may be a group-level Number of Colonies 2 feature that enhances the fitness of colony members. The selective importance of avoiding queen movement remains 0 Reunited Reunited Did not speculative until we can measure the actual risks to the at nest at queenless reunite queen at different phases of emigration. with queen nest The queen’s location is not the only determining factor in reunification, as shown by our second experiment. When divided between two sites that differed in interior light level, Fig. 2 Results of Experiment 1. Bar heights give the total number of colonies reuniting at the nest containing the queen, reuniting at the nest colonies consistently chose the darker nest, even though this without the queen, or failing to reunite required them to move the queen from the brighter nest. The 123 Queen location and nest site preference influence colony reunification by the ant… functional consequences of a nest’s light level on colony current site and that of the new one (Dornhaus et al. 2004). If survival and reproduction are unknown, but previous the improvement is too small, it will not justify the costs of observations make clear that Temnothorax colonies con- emigration. Similar calculations may come into play during sistently prefer dimmer nests (Franks et al. 2003b). A reunification, leading some colonies to avoid the costs of reasonable assumption is that dimness is an indicator of site transporting half the colony to a new home. Division might quality, because a dim cavity likely has a solid wall with few have been favored in our experiments by the short distance breaches and a small, defensible entrance (Franks et al. between nests, which could make it easier for the two por- 2006). If so, we can interpret the choices we observed as a tions of the colony to remain in contact and function as a prioritization of long-term colony wellbeing over protection single entity. of the queen from a short-term risk. The optimal choice Division also occurs in natural settings, either as a likely depends on the relative costs and benefits of each method of reproduction or as a strategy of seasonal poly- option. If faced with a small difference in site quality, the domy. Several species of Temnothorax show evidence of ants might do better by accepting a slightly inferior nest to polydomy (Alloway et al. 1982; Stuart 1985; Partridge et al. minimize risk to their queen. Future experiments should test 1997; Roberts et al. 1999); in T. albipennis and T. tuberum, a range of quality differences to examine this possibility. colonies appear to divide among multiple nests during the Queen location and nest dimness are not the only features spring and summer, but reunite in a single nest over the likely to influence reunification. Ants show clear prefer- winter (Partridge et al. 1997; Roberts et al. 1999). Polydomy ences for a range of site attributes, including cavity size and can prevent overcrowding and enhance foraging efficiency shape, entrance size, and contextual factors such as food during the growing season (Debout et al. 2007; Lanan et al. availability and the presence of competitors, predators, or 2011; Cao 2013; Stroeymeyt et al. 2014; Robinson 2014). other hazards (Pratt and Pierce 2001; Franks et al. Reuniting at a single nest in winter can improve defense and 2003a, b, 2007; Evison et al. 2012; Cao and Dornhaus 2012; environmental regulation during winter cold (Partridge et al. Minter et al. 2013; Enrı´quez et al. 2013; Sasaki et al. 2014; 1997; Roberts et al. 1999; Stroeymeyt et al. 2014). These Pontieri et al. 2014). Colonies somehow integrate these seasonal shifts present another context, in addition to features when choosing among sites, and appear to weight migration, where the ability to reunify may be important to a them differently, presumably on the basis of their relative colony. In T. rugatulus, the occurrence of seasonal poly- importance to nest function (Franks et al. 2003b; Sasaki and domy remains unexplored, but laboratory observations Pratt 2013). It is reasonable to assume that ants similarly show that crowded conditions can induce colonies to divide attend to these attributes when reunifying after splitting among multiple nest sites (Cao 2013). Polydomy may also between sites. In addition to the site features themselves, intersect with variation in queen number in this species. ants may be influenced by the distribution of colony mem- These ants are facultatively polygynous and possess two bers across sites. We took care to ensure that site distinct queen morphs: larger macrogynes that disperse to populations were equal in our experiments, but differences found nests independently and smaller microgynes that are are likely to arise in actual emigrations and may influence re-adopted into their natal nests (Ru¨ppell et al. 2001). the ants’ choice of where to settle. Colonies might benefit Variation among colonies in queen type and number are from choosing the most populous site, thus minimizing the potentially associated with differences in reunification number of ants that must be moved and exposed to external behavior. For example, polygynous colonies may be less risks. Population could also serve as a symmetry breaker sensitive to pressures to remain monodomous, and, when when sites are not otherwise well distinguished. Even with forcibly divided, we can speculate that they might reunite very simple rules, such as dependence of transport initiation less frequently than monogynous colonies. on a site’s current population, the colony could quickly The findings reported here expand the study of colony amplify a small initial difference in population into con- emigration to the problem of reunification, a previously sensus on a single site. Similar effects have been shown to neglected aspect of consensus building. Temporary splits account for collective selection of a single aggregation site like the ones we created in the laboratory are likely to occur (Jeanson et al. 2004, 2005). frequently in the life histories of ants, given the high fre- Most of the colonies that we split reunited, but a portion quency with which many species migrate (Ho¨lldobler and did not, even after 20 h. These colonies might eventually Wilson 1990; McGlynn 2012). We focused here on the have reunited if given more time, but their behavior can also criteria that determine a colony’s final choice of home, or be interpreted as a decision to remain separated. Reunifi- whether to reunite at all. Another critical aspect of reunifi- cation, like any migration, involves risks that colonies cation is the behavioral mechanism by which colonies weigh when deciding whether to move. For example, when accomplish the challenging tasks of selecting a single site a colony is given the opportunity to move into a better nest, and coordinating the movement of their members to it. The its probability of doing so depends both on the quality of its same behavioral tactics that underlie emigration and 123 G. N. Doering, S. C. Pratt collective choice—including individual quality assessment, Franks NR, Pratt SC, Mallon EB et al (2002) Information flow, opinion nestmate recruitment, and quorum rules—are likely to be polling and collective intelligence in house-hunting social insects. Philos Trans R Soc B Biol Sci 357:1567–1583. doi:10.1098/rstb. important here as well, but other novel aspects of collective 2002.1066 behavior may also come to light. Franks NR, Dornhaus A, Fitzsimmons JP, Stevens M (2003a) Speed versus accuracy in collective decision making. Proc R Soc B Biol Acknowledgments This research was supported by the United States Sci 270:2457–2463. doi:10.1098/rspb.2003.2527 National Science Foundation (Award CCF-1012029). Franks NR, Mallon EB, Bray HE et al (2003b) Strategies for choosing between alternatives with different attributes: exemplified by house-hunting ants. 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